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Globally Distributed Root Endophyte Phialocephala Subalpina Links Schlegel et al. BMC Genomics (2016) 17:1015 DOI 10.1186/s12864-016-3369-8 RESEARCH ARTICLE Open Access Globally distributed root endophyte Phialocephala subalpina links pathogenic and saprophytic lifestyles Markus Schlegel1†, Martin Münsterkötter2†, Ulrich Güldener2,3, Rémy Bruggmann4, Angelo Duò1, Matthieu Hainaut5, Bernard Henrissat5, Christian M. K. Sieber2,6, Dirk Hoffmeister7 and Christoph R. Grünig1,8* Abstract Background: Whereas an increasing number of pathogenic and mutualistic ascomycetous species were sequenced in the past decade, species showing a seemingly neutral association such as root endophytes received less attention. In the present study, the genome of Phialocephala subalpina, the most frequent species of the Phialocephala fortinii s.l. – Acephala applanata species complex, was sequenced for insight in the genome structure and gene inventory of these wide-spread root endophytes. Results: The genome of P. subalpina was sequenced using Roche/454 GS FLX technology and a whole genome shotgun strategy. The assembly resulted in 205 scaffolds and a genome size of 69.7 Mb. The expanded genome size in P. subalpina was not due to the proliferation of transposable elements or other repeats, as is the case with other ascomycetous genomes. Instead, P. subalpina revealed an expanded gene inventory that includes 20,173 gene models. Comparative genome analysis of P. subalpina with 13 ascomycetes shows that P. subalpina uses a versatile gene inventory including genes specific for pathogens and saprophytes. Moreover, the gene inventory for carbohydrate active enzymes (CAZymes) was expanded including genes involved in degradation of biopolymers, such as pectin, hemicellulose, cellulose and lignin. Conclusions: The analysis of a globally distributed root endophyte allowed detailed insights in the gene inventory and genome organization of a yet largely neglected group of organisms. We showed that the ubiquitous root endophyte P. subalpina has a broad gene inventory that links pathogenic and saprophytic lifestyles. Keywords: Comparative genomics, Lifestyle, Root endophyte, Species complex, Parasitism-mutualism continuum Background nature of interaction with their hosts [5, 6]. It is assumed Plant roots are confronted with the colonization of symbi- that they behave along the mutualism - antagonism con- otic fungal species ranging from pathogens to mutualists tinuum depending on host conditions and environment, [1]. While research has largely been focused on the symbi- as shown for some mycorrhizal fungi [7–9]. otic and pathogenic interactions, seemingly neutral associ- Species belonging to the helotialean Phialocephala for- ations with plant roots by endophytes received less tinii s.l. – Acephala applanata species complex (PAC) attention [2, 3]. Endophytic fungi colonize functional roots are the dominant root endophytes in woody plant spe- tissues but disease symptoms do not develop at all or at cies [5]. PAC shows a global distribution as PAC species least not for prolonged periods of time [4]. Despite their colonize roots from arctic to subtropical plant species prevalence in many ecosystems, little is known about the throughout the northern hemisphere [10–12]. Recently, a study proved the presence of PAC on the southern * Correspondence: [email protected] hemisphere [13]. In contrast to ectomycorrhizal species †Equal contributors (EcM), which are usually confined to primary, non- 1 Institute of Integrative Biology (IBZ), Forest Pathology and Dendrology, ETH lignified roots, PAC can be found in all parts of the root Zürich, 8092 Zürich, Switzerland 8Microsynth AG, Schützenstrasse 15, 9436 Balgach, Switzerland system, predominatly on fine roots < 3 mm where up to Full list of author information is available at the end of the article © The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Schlegel et al. BMC Genomics (2016) 17:1015 Page 2 of 22 80% of randomly sampled roots were colonized [5]. In They were described as beneficial, neutral or pathogenic addition, PAC species are belonging to the first colo- for different hosts, growing conditions and fungal strains nizers of tree seedlings in natural forest ecosystems, in- [5, 20, 21]. New results comparing the effect of PAC spe- fecting them within a few weeks after germination [14]. cies and strains on Picea abies indicate that the outcome PAC is composed of more than 15 cryptic species [10], of the interactions is mainly driven by the fungal genotype eight of which were formally described [15, 16]. Among and follow the antagonism-mutualism continuum. the strains sampled from a single study site, PAC species Whereas some of the PAC/P. subalpina strains were form communities of up to 10 sympatrically occurring shown to be pathogenic and killed most of the seedlings, species. In contrast to agricultural ecosystems, PAC others were benign [22]. Nevertheless, infection by PAC is communities remain stable for several years [17] al- costly for the plant since an increase in plant growth was though minor long-term changes in the frequency of never observed [22]. The outcome of PAC-host interac- species can be observed [18]. Most PAC communities tions depends on the ability of PAC strains to invade and are dominated by few species and additional species colonize host root tissues. This is evident by the health occur at low frequencies [5] as observed in many other status of Norway spruce seedlings, which negatively corre- community structures of biological systems [19]. Species lates with the biomass of the fungus in roots [22, 23]. diversity and community structure do not correlate with However, negative effects of harmful PAC strains are re- the tree community, geographical location, soil proper- duced by the co-colonization of ectomycorrhizal fungi ties, management practices nor does climate, precipita- and other PAC strains [24]. tion and temperature [10]. Host specificity of PAC The dynamics of PAC-host colonization was rarely stud- species was not observed [5] except for A. applanata ied [25–27], and data on intraspecific variation of that was almost exclusively isolated from species belong- colonization dynamics for different PAC species is missing ing to the Pinaceae but rarely from ericaceous roots of completely. In general, PAC strains form hyphopodia- or the ground vegetation [14]. appressoria-like structures to enter root hairs or epidermal Despite the fact that PAC species are highly successful cells (Fig. 1a, b). After entering the root, PAC strains grow colonizers of plant roots and widely distributed in natural inter- and intracellularly and colonize the cortex but rarely ecosystems, their ecological role is still poorly understood. invade the vascular cylinder (Fig. 1c, d). Intercellular ab 10 µm 2 µm cd 10 µm 2 µm Fig. 1 Key features of the colonization of roots by PAC species. Key steps in the colonization of roots by PAC species (V. Queloz, unpublished). Figure 1a, b. Surface colonization and appressoria/hyphopodia formation of P. subalpina on Cistus incanus roots. Figure 1c. Cross-section of Pinus strobus root colonized by PAC stained using borax, methylene blue and toluidine blue and counterstained with basic fuchsine. The fungus com- pletely colonizes the cortical tissue up to the endodermis. Accumulation of phenolic compounds in the vascular cylinder is evident by the pres- ence of dark granular structures. Figure 1d. Example of intracellular colonization of P. subalpina in C. incanus cortex (arrow) Schlegel et al. BMC Genomics (2016) 17:1015 Page 3 of 22 labyrinthine fungal tissue resembling the Hartig net in ecto- Table 1 Genome statistics for Phialocephala subalpina mycorrhizal fungi as well as mantel-like structures were oc- Genome size [Mb] 69.69 – casionally observed for PAC [27 29]. Scaffolds 205 Host defense reactions such as cell-wall appositions or Scaffolds N50 [kb] 1,449 lignituber formation were rarely observed [27]. Intracel- N50 number of scaffolds 16 lular hyphae traverse host cells by narrow penetration hyphae without apparent lysis of the plant cell wall while GC (%) 45.9 the host cell cytoplasma disintegrates after colonization Predicted protein-coding genes 20,173 by PAC hyphae (Fig. 1d). Pertaining to the ultrastruc- Average exon length [bp] 443.9 tural level, hyphae are not surrounded by host-derived Average intron length [bp] 80.2 perifungal membranes, which are regarded as hallmark Average number of introns per gene 2.7 for biotrophic fungal associations [27]. Finally, cortical tRNAs 91 cells of the plant are often associated with thick-walled, heavily melanized fungal cells, i.e. microsclerotia, which TEs content 5.70% were shown to accumulate reserve substances [5, 25]. Other repeatsa 8.10% The availability of genomic sequences provides informa- atandem repeats, SSR, and low-complexity DNA tion on the gene inventory of species and identifies char- acteristic genomic structures and gene sets associated FJOG01000001-FJOG01000205). Mapping of reads data with different lifestyles
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